Five Decades of Data Yield No Support for Adaptive Biasing of Offspring Sex Ratio in Wild Baboons (Papio cynocephalus).

AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n=1,372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

Evaluating expert-based habitat suitability information of terrestrial mammals with GPS-tracking data.

Aim: Macroecological studies that require habitat suitability data for many species often derive this information from expert opinion. However, expert-based information is inherently subjective and thus prone to errors. The increasing availability of GPS tracking data offers opportunities to evaluate and supplement expert-based information with detailed empirical evidence. Here, we compared expert-based habitat suitability information from the International Union for Conservation of Nature (IUCN) with habitat suitability information derived from GPS-tracking data of 1,498 individuals from 49 mammal species. Location: Worldwide. Time period: 1998-2021. Major taxa studied: Forty-nine terrestrial mammal species. Methods: Using GPS data, we estimated two measures of habitat suitability for each individual animal: proportional habitat use (proportion of GPS locations within a habitat type), and selection ratio (habitat use relative to its availability). For each individual we then evaluated whether the GPS-based habitat suitability measures were in agreement with the IUCN data. To that end, we calculated the probability that the ranking of empirical habitat suitability measures was in agreement with IUCN's classification into suitable, marginal and unsuitable habitat types. Results: IUCN habitat suitability data were in accordance with the GPS data (> 95% probability of agreement) for 33 out of 49 species based on proportional habitat use estimates and for 25 out of 49 species based on selection ratios. In addition, 37 and 34 species had a > 50% probability of agreement based on proportional habitat use and selection ratios, respectively. Main conclusions: We show how GPS-tracking data can be used to evaluate IUCN habitat suitability data. Our findings indicate that for the majority of species included in this study, it is appropriate to use IUCN habitat suitability data in macroecological studies. Furthermore, we show that GPS-tracking data can be used to identify and prioritize species and habitat types for re-evaluation of IUCN habitat suitability data.

Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

Mechanisms of inbreeding avoidance in a wild primate.

Inbreeding often imposes net fitness costs,1-5 leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.4-9 However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,6 and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.9 These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.9.

Glucocorticoid exposure predicts survival in female baboons.

Are differences in hypothalamic-pituitary-adrenal (HPA) axis activation across the adult life span linked to differences in survival? This question has been the subject of considerable debate. We analyze the link between survival and fecal glucocorticoid (GC) measures in a wild primate population, leveraging an unusually extensive longitudinal dataset of 14,173 GC measurements from 242 adult female baboons over 1634 female years. We document a powerful link between GCs and survival: Females with relatively high current GCs or high lifelong cumulative GCs face an elevated risk of death. A hypothetical female who maintained GCs in the top 90% for her age across adulthood would be expected to lose 5.4 years of life relative to a female who maintained GCs in the bottom 10% for her age. Hence, differences among individuals in HPA axis activity provide valuable prognostic information about disparities in life span.

Maternal death and offspring fitness in multiple wild primates.

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

A comparison of dominance rank metrics reveals multiple competitive landscapes in an animal society.

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes and reproductive performance. Studies of how dominance rank predicts these traits typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here, we compare the ability of two dominance rank metrics-simple ordinal rank and proportional or 'standardized' rank-to predict 20 traits in a wild baboon population in Amboseli, Kenya. We propose that simple ordinal rank best predicts traits when competition is density-dependent, whereas proportional rank best predicts traits when competition is density-independent. We found that for 75% of traits (15/20), one rank metric performed better than the other. Strikingly, all male traits were best predicted by simple ordinal rank, whereas female traits were evenly split between proportional and simple ordinal rank. Hence, male and female traits are shaped by different competitive processes: males are largely driven by density-dependent resource access (e.g. access to oestrous females), whereas females are shaped by both density-independent (e.g. distributed food resources) and density-dependent resource access. This method of comparing how different rank metrics predict traits can be used to distinguish between different competitive processes operating in animal societies.

Higher dominance rank is associated with lower glucocorticoids in wild female baboons: A rank metric comparison.

In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.

Social bonds do not mediate the relationship between early adversity and adult glucocorticoids in wild baboons.

In humans and other animals, harsh conditions in early life can have profound effects on adult physiology, including the stress response. This relationship may be mediated by a lack of supportive relationships in adulthood. That is, early life adversity may inhibit the formation of supportive social ties, and weak social support is itself often linked to dysregulated stress responses. Here, we use prospective, longitudinal data from wild baboons in Kenya to test the links between early adversity, adult social bonds, and adult fecal glucocorticoid hormone concentrations (a measure of hypothalamic-pituitary-adrenal [HPA] axis activation and the stress response). Using a causal inference framework, we found that experiencing one or more sources of early adversity led to a 9 to 14% increase in females' glucocorticoid concentrations across adulthood. However, these effects were not mediated by weak social bonds: The direct effects of early adversity on adult glucocorticoid concentrations were 11 times stronger than the effects mediated by social bonds. This pattern occurred, in part, because the effect of social bonds on glucocorticoids was weak compared to the powerful effects of early adversity on glucocorticoid levels in adulthood. Hence, in female baboons, weak social bonds in adulthood are not enough to explain the effects of early adversity on glucocorticoid concentrations. Together, our results support the well-established notions that early adversity and weak social bonds both predict poor adult health. However, the magnitudes of these two effects differ considerably, and they may act independently of one another.

Effects of body size on estimation of mammalian area requirements.

Accurately quantifying species' area requirements is a prerequisite for effective area-based conservation. This typically involves collecting tracking data on species of interest and then conducting home-range analyses. Problematically, autocorrelation in tracking data can result in space needs being severely underestimated. Based on the previous work, we hypothesized the magnitude of underestimation varies with body mass, a relationship that could have serious conservation implications. To evaluate this hypothesis for terrestrial mammals, we estimated home-range areas with global positioning system (GPS) locations from 757 individuals across 61 globally distributed mammalian species with body masses ranging from 0.4 to 4000 kg. We then applied block cross-validation to quantify bias in empirical home-range estimates. Area requirements of mammals <10 kg were underestimated by a mean approximately15%, and species weighing approximately100 kg were underestimated by approximately50% on average. Thus, we found area estimation was subject to autocorrelation-induced bias that was worse for large species. Combined with the fact that extinction risk increases as body mass increases, the allometric scaling of bias we observed suggests the most threatened species are also likely to be those with the least accurate home-range estimates. As a correction, we tested whether data thinning or autocorrelation-informed home-range estimation minimized the scaling effect of autocorrelation on area estimates. Data thinning required an approximately93% data loss to achieve statistical independence with 95% confidence and was, therefore, not a viable solution. In contrast, autocorrelation-informed home-range estimation resulted in consistently accurate estimates irrespective of mass. When relating body mass to home range size, we detected that correcting for autocorrelation resulted in a scaling exponent significantly >1, meaning the scaling of the relationship changed substantially at the upper end of the mass spectrum.

Efectos del Tamaño Corporal sobre la Estimación de los Requerimientos de Área de Mamíferos Resumen La cuantificación precisa de los requerimientos de área de una especie es un prerrequisito para que la conservación basada en áreas sea efectiva. Esto comúnmente implica la recolección de datos de rastreo de la especie de interés para después realizar análisis de la distribución local. De manera problemática, la autocorrelación en los datos de rastreo puede resultar en una subestimación grave de las necesidades de espacio. Con base en trabajos previos, formulamos una hipótesis en la que supusimos que la magnitud de la subestimación varía con la masa corporal, una relación que podría tener implicaciones serias para la conservación. Para probar esta hipótesis en mamíferos terrestres, estimamos las áreas de distribución local con las ubicaciones en GPS de 757 individuos de 61 especies de mamíferos distribuidas mundialmente con una masa corporal entre 0.4 y 4,000 kg. Después aplicamos una validación cruzada en bloque para cuantificar el sesgo en estimaciones empíricas de la distribución local. Los requerimientos de área de los mamíferos <10 kg fueron subestimados por una media ∼15% y las especies con una masa ∼100 kg fueron subestimadas en ∼50% en promedio. Por lo tanto, encontramos que la estimación del área estaba sujeta al sesgo inducido por la autocorrelación, el cual era peor para las especies de talla grande. En combinación con el hecho de que el riesgo de extinción incrementa conforme aumenta la masa corporal, el escalamiento alométrico del sesgo que observamos sugiere que la mayoría de las especies amenazadas también tienen la probabilidad de ser aquellas especies con las estimaciones de distribución local menos acertadas. Como corrección, probamos si la reducción de datos o la estimación de la distribución local informada por la autocorrelación minimizan el efecto de escalamiento que tiene la autocorrelación sobre las estimaciones de área. La reducción de datos requirió una pérdida de datos del ∼93% para lograr la independencia estadística con un 95% de confianza y por lo tanto no fue una solución viable. Al contrario, la estimación de la distribución local informada por la autocorrelación resultó en estimaciones constantemente precisas sin importar la masa corporal. Cuando relacionamos la masa corporal con el tamaño de la distribución local, detectamos que la corrección de la autocorrelación resultó en un exponente de escalamiento significativamente >1, lo que significa que el escalamiento de la relación cambió sustancialmente en el extremo superior del espectro de la masa corporal.

Intergenerational effects of early adversity on survival in wild baboons.

Early life adversity can affect an individual's health, survival, and fertility for many years after the adverse experience. Whether early life adversity also imposes intergenerational effects on the exposed individual's offspring is not well understood. We fill this gap by leveraging prospective, longitudinal data on a wild, long-lived primate. We find that juveniles whose mothers experienced early life adversity exhibit high mortality before age 4, independent of the juvenile's own experience of early adversity. These juveniles often preceded their mothers in death by 1 to 2 years, indicating that high adversity females decline in their ability to raise offspring near the end of life. While we cannot exclude direct effects of a parent's environment on offspring quality (e.g., inherited epigenetic changes), our results are completely consistent with a classic parental effect, in which the environment experienced by a parent affects its future phenotype and therefore its offspring's phenotype.

Interbirth intervals in wild baboons: Environmental predictors and hormonal correlates.

OBJECTIVES: Interbirth intervals (IBIs) are a key metric of female reproductive success; understanding how they are regulated by environmental, social, and demographic factors can provide insight into sources of variance in female fitness. MATERIALS AND METHODS: Using 36 years of reproductive data on 490 IBIs for 160 wild female baboons, we identified sources of variance in the duration of IBIs and of their component phases: postpartum amenorrhea (PPA), sexual cycling, and pregnancy. We also examined how body fat and fecal hormone concentrations varied during female IBIs. RESULTS: We found that IBIs tended to be shorter (reproduction was accelerated) when female traits and environmental variables promoted energy acquisition, but with different specific effects for different component phases of the IBI. We also found that females lost a substantial amount of body fat during PPA, indicating that PPA imposes accumulating energetic costs as it progresses. Prior to cycle resumption females began to regain body fat; body fat was stable across the cycling phase and increased throughout most of pregnancy. However, body fat scores per se were not associated with the duration of any of the component phases. Finally, we found that fecal glucocorticoid concentrations decreased as PPA progressed, suggesting a decline in energetic stress over this phase. Fecal progestogen and estrogen concentrations changed over time during sexual cycling; the direction of these changes depended on the phase of the sexual cycle (luteal versus early or late follicular phases). DISCUSSION: Our study lends insight into the energetic constraints on female primate reproduction, revealing how female environments, changes in body fat, and steroid hormone concentrations relate to IBI duration and to reproductive readiness.

Hormonal correlates of natal dispersal and rank attainment in wild male baboons.

In many mammals, maturational milestones such as dispersal and the attainment of adult dominance rank mark stages in the onset of reproductive activity and depend on a coordinated set of hormonal and socio-behavioral changes. Studies that focus on the link between hormones and maturational milestones are uncommon in wild mammals because of the challenges of obtaining adequate sample sizes of maturing animals and of tracking the movements of dispersing animals. We examined two maturational milestones in wild male baboons-adult dominance rank attainment and natal dispersal-and measured their association with variation in glucocorticoids (fGC) and fecal testosterone (fT). We found that rank attainment is associated with an increase in fGC levels but not fT levels: males that have achieved any adult rank have higher fGC than males that have not yet attained an adult rank. This indicates that once males have attained an adult rank they experience greater energetic and/or psychosocial demands than they did prior to attaining this milestone, most likely because of the resulting participation in both agonistic and sexual behaviors that accompany rank attainment. In contrast, natal dispersal does not produce sustained increases in either fGC or fT levels, suggesting that individuals are either well adapted to face the challenges associated with dispersal or that the effects of dispersal on hormone levels are ephemeral for male baboons.

Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.

Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.

Conditional fetal and infant killing by male baboons.

Sexually selected feticide-the death of infants in utero as a result of male behaviour-has only rarely been described or analysed, although it is presumed to be favoured by the same selective pressures that favour sexually selected infanticide. To test this hypothesis, we measured the frequency of feticide and infanticide by male baboons of the Amboseli basin in Kenya, and examined which characteristics of a male and his environment made him more likely to commit feticide and/or infanticide. We found a dramatic increase in fetal and infant death rates, but no increase in death rates of 1- to 2-year-old individuals, following the immigration of males who stood to benefit from feticide and infanticide. Specifically, fetal and infant death rates were highest following immigrations in which: (i) the immigrant male rapidly attained high rank, (ii) that male remained consistently resident in the group for at least three months, (iii) food availability and social group range overlap was relatively low and (iv) relatively many pregnant females and/or dependent infants were present. Together, these results provide strong evidence for the existence of both sexually selected feticide and infanticide in our population, and they indicate that feticide and infanticide are conditional male behavioural strategies employed under particular circumstances.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Cumulative early life adversity predicts longevity in wild baboons.

In humans and other animals, harsh circumstances in early life predict morbidity and mortality in adulthood. Multiple adverse conditions are thought to be especially toxic, but this hypothesis has rarely been tested in a prospective, longitudinal framework, especially in long-lived mammals. Here we use prospective data on 196 wild female baboons to show that cumulative early adversity predicts natural adult lifespan. Females who experience ≥3 sources of early adversity die a median of 10 years earlier than females who experience ≤1 adverse circumstances (median lifespan is 18.5 years). Females who experience the most adversity are also socially isolated in adulthood, suggesting that social processes partially explain the link between early adversity and adult survival. Our results provide powerful evidence for the developmental origins of health and disease and indicate that close ties between early adversity and survival arise even in the absence of health habit and health care-related explanations.

Female and male life tables for seven wild primate species.

We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica; baboon (Papio cynocephalus) and blue monkey (Cercopithecus mitis) in Kenya; chimpanzee (Pan troglodytes) in Tanzania; and gorilla (Gorilla beringei) in Rwanda. Using one-year age-class intervals, we computed point estimates of age-specific survival for both sexes. In all species, our survival estimates for the dispersing sex are affected by heavy censoring. We also calculated reproductive value, life expectancy, and mortality hazards for females. We used bootstrapping to place confidence intervals on life-table summary metrics (R0, the net reproductive rate; λ, the population growth rate; and G, the generation time). These data have high potential for reuse; they derive from continuous population monitoring of long-lived organisms and will be invaluable for addressing questions about comparative demography, primate conservation and human evolution.

Resource base influences genome-wide DNA methylation levels in wild baboons (Papio cynocephalus).

Variation in resource availability commonly exerts strong effects on fitness-related traits in wild animals. However, we know little about the molecular mechanisms that mediate these effects, or about their persistence over time. To address these questions, we profiled genome-wide whole-blood DNA methylation levels in two sets of wild baboons: (i) 'wild-feeding' baboons that foraged naturally in a savanna environment and (ii) 'Lodge' baboons that had ready access to spatially concentrated human food scraps, resulting in high feeding efficiency and low daily travel distances. We identified 1014 sites (0.20% of sites tested) that were differentially methylated between wild-feeding and Lodge baboons, providing the first evidence that resource availability shapes the epigenome in a wild mammal. Differentially methylated sites tended to occur in contiguous stretches (i.e., in differentially methylated regions or DMRs), in promoters and enhancers, and near metabolism-related genes, supporting their functional importance in gene regulation. In agreement, reporter assay experiments confirmed that methylation at the largest identified DMR, located in the promoter of a key glycolysis-related gene, was sufficient to causally drive changes in gene expression. Intriguingly, all dispersing males carried a consistent epigenetic signature of their membership in a wild-feeding group, regardless of whether males dispersed into or out of this group as adults. Together, our findings support a role for DNA methylation in mediating ecological effects on phenotypic traits in the wild and emphasize the dynamic environmental sensitivity of DNA methylation levels across the life course.